Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T01:28:47.797Z Has data issue: false hasContentIssue false

Cholesterol crystallization in gall-bladder bile of pigs given cholesterol–β-cyclodextrin-enriched diets with either casein or soyabean concentrate as protein sources

Published online by Cambridge University Press:  09 March 2007

Isabelle Catala
Affiliation:
Unité d'Ecologie et de Physiologie du Système Digestif, Bâtiment 405, INRA, 78352 Jouy-en-Josas Cedex, France Health and Nutrition Service, Eridania Béghin-Say, Vilvoorde, Belgium
Catherine Juste*
Affiliation:
Unité d'Ecologie et de Physiologie du Système Digestif, Bâtiment 405, INRA, 78352 Jouy-en-Josas Cedex, France
Nathalie Boehler
Affiliation:
Laboratoire de Physiologie de la Nutrition, Université Paris XI, 91405 Orsay Cedex, France
Jacqueline Férézou
Affiliation:
Laboratoire de Physiologie de la Nutrition, Université Paris XI, 91405 Orsay Cedex, France
Marc André
Affiliation:
U476, Nutrition Humaine et Lipides, INSERM, 18 avenue Mozart, 13009 Marseille, France
Michel Riottot
Affiliation:
Laboratoire de Physiologie de la Nutrition, Université Paris XI, 91405 Orsay Cedex, France
Claude Lutton
Affiliation:
Laboratoire de Physiologie de la Nutrition, Université Paris XI, 91405 Orsay Cedex, France
Huguette Lafont
Affiliation:
U476, Nutrition Humaine et Lipides, INSERM, 18 avenue Mozart, 13009 Marseille, France
Francis Bornet
Affiliation:
Health and Nutrition Service, Eridania Béghin-Say, Vilvoorde, Belgium
Tristan Corring
Affiliation:
Unité d'Ecologie et de Physiologie du Système Digestif, Bâtiment 405, INRA, 78352 Jouy-en-Josas Cedex, France
*
*Corresponding author: Dr Catherine Juste, fax +33 1 34 65 24 92, email juste@jouy.inra.fr
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Cholesterol precipitation from supersaturated bile is the earliest and determinant step in the formation of cholesterol gallstones, which is thought to be diet-dependent. Bile composition, appearance and growth of cholesterol crystals were studied in fresh gall-bladder biles from pigs adapted to four different protein-containing diets over 3 weeks: 160 g dietary protein/kg as casein (C16; n 6), or as soyabean-protein concentrate (S16; n 6), or a mixture of both protein sources (casein–soyabean protein, 70 : 30, w/w) (CS16;n 6), or 320 g of the mixed protein/kg (CS32; n 6). Moreover, all four diets contained 3 g cholesterol/kg and 50 g β-cyclodextrin/kg as modifiers of bile composition towards cholesterol pro-crystallization. Cholesterol precipitation was most active after the high-protein diet, CS32, and the casein diet, C16, and lowest after the soyabean-protein diet, S16. It was intermediate after the mixed diet, CS16, but still much lower than in the former two groups. These diet-induced variations were suggested to be mediated through modifications in the biliary profile of bile acids, whereas all other biliary constituents studied were essentially unchanged. The fasting level of plasma cholesterol was lowest in both 160 g protein/kg diets containing soyabean protein (S16 and CS16), highest for the high-protein diet CS32, and intermediate for the C16 diet. These results should encourage clinical studies on the effect of soyabean protein, or other vegetable proteins, for primary or recurrence prevention of cholelithiasis at its earliest stage.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Aldini, R, Roda, A, Montagnani, MCerrè, C, Pellicciari, R and Roda, E (1996) Relationship between structure and intestinal absorption of bile acids with a steroid or side-chain modification. Steroids 61, 590597.CrossRefGoogle ScholarPubMed
Anderson, RL and Wolf, WJ (1995) Compositional changes in trypsin inhibitors, phytic acid, saponins, and isoflavones related to soybean processing. Journal of Nutrition 125, 581S588S.Google ScholarPubMed
Attili, AF, Scafato, E, Marchioli, R, Marfisi, RM and Festi, D (1998) Diet and gallstones in Italy: the cross-sectional MICOL results. Hepatology 27, 14921498.CrossRefGoogle ScholarPubMed
Beynen, AC (1990) Mode of cholesterolemic action of dietary proteins. Monographs on Atherosclerosis 16, 153159.Google ScholarPubMed
Beynen, AC (1990) Comparison of the mechanisms proposed to explain the hypocholesterolemic effect of soybean protein versus casein in experimental animals. Journal of Nutritional Science and Vitaminology 53, 11911196.Google Scholar
Beynen, AC, West, CE, Spaaij, CJK, Huisman, JVan Leeuwen, P, Schutte, JB and Hackeng, WHL (1990) Cholesterol metabolism, digestion rates and postprandial changes in serum of swine fed purified diets containing either casein or soybean protein. Journal of Nutrition 120, 422430.CrossRefGoogle ScholarPubMed
Booker, ML, Scott, TE and La Morte, WW (1989) Effect of dietary cholesterol on phosphatidylcholines and phosphatidylethanolamines in bile and gallbladder mucosa in the prairie dog. Gastroenterology 97, 12611267.CrossRefGoogle ScholarPubMed
Booker, ML, Scott, TE and La Morte, WW (1990) Effects of dietary fish oil on biliary phospholipids and prostaglandin synthesis in the cholesterol-fed prairie dog. Lipids 25, 2732.CrossRefGoogle ScholarPubMed
Bouvier, A and Huet, S (1994) nls2 Non-linear regression by s-plus functions. Computational Statistics and Data Analysis 18, 187190.CrossRefGoogle Scholar
Carolibosc, FX, Deveau, C, Peten, EP, Delabre, B, Zanaldi, H, Hebuterne, X, Hastier, P, Viudes, F, Belanger, F, Carolibosc, C, Harris, A, Hardison, M, Rampal, P and Delmont, JP (1998) Cholelithiasis and dietary risk factors: an epidemiologic investigation in Vidauban, Southeast France. Digestive Diseases and Sciences 43, 21312137.CrossRefGoogle ScholarPubMed
Carroll, KK (1991) Review of clinical studies on cholesterol-lowering response to soy protein. Journal of the American Dietetics Association 91, 820827.CrossRefGoogle ScholarPubMed
Catala, I, Domingo, N, Juste, CGueugneau, A-M, Thorin, B, Lutton, C, Corring, T and Lafont, H (1998) Effect of β-cyclodextrin dietary supplementation on biliary proteins and their resulting cholesterol nucleating activity in pigs. Biochimica et Biophysica Acta 1394, 7484.CrossRefGoogle ScholarPubMed
Council for International Organisations of Medical Sciences (1986) International guiding principles for biomedical research involving animals issued by CIOMS. Veterinary Quarterly 8, 350352.CrossRefGoogle Scholar
Donovan, JM, Timofeyeva, N and Carey, MC (1989) Cholesterol monohydrate (ChM) and liquid crystal formation in model biles: effects of bile acids (BS) hydrophobicity and phosphatidylcholine (PC) contents. Hepatology 10, A598.Google Scholar
Dusserre, JP, Montet, AM and Montet, JC (1988) Effect of hyocholic acid on the prevention and dissolution of biliary cholesterol crystals in mice. Canadian Journal of Physiology and Pharmacology 66, 10281034.CrossRefGoogle ScholarPubMed
Erdman, JW and Fordyce, E (1989) Soy products and the human diet. American Journal of Clinical Nutrition 49, 725737.CrossRefGoogle ScholarPubMed
Férézou, J, Riottot, M, Sérougne, C, Cohen-Solal, C, Catala, I, Alquier, C, Parquet, M, Juste, C, Lafont, HMathé, D, Corring, T and Lutton, C (1997) Hypocholesterolemic action of β-cyclodextrin and its effects on cholesterol metabolism in pigs fed a cholesterol-enriched diet. Journal of Lipid Research 38, 86100.CrossRefGoogle ScholarPubMed
Folch, J, Lees, M and Sloane-Stanley, GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry 226, 497509.CrossRefGoogle ScholarPubMed
Fumagalli, R, Soleri, L, Farini, R, Musanti, R, Mantero, O, Noseda, G, Gatti, E and Sirtori, CR (1982) Fecal cholesterol excretion studies in type II hypercholesterolemic patients treated with soybean protein diet. Atherosclerosis 43, 341353.CrossRefGoogle ScholarPubMed
Halpern, Z, Moshkowitz, M, Laufer, H, Peled, Y and Gilat, T (1993) Effect of phospholipids and their molecular species on cholesterol solubility and nucleation in human and model bile. Gut 34, 110115.CrossRefGoogle Scholar
Hay, DW and Carey, MC (1990) Pathophysiology and pathogenesis of cholesterol gallstone formation. Seminars in Liver Disease 10, 159170.CrossRefGoogle ScholarPubMed
Hayes, KC, Livingston, A and Trautwein, EA (1992) Dietary impact on biliary lipids and gallstones. Annual Review of Nutrition 12, 299326.CrossRefGoogle ScholarPubMed
Heaton, KW (1984) The role of diet in the aetiology of cholelithiasis. Nutrition Abstracts and Reviews 54, 549560.Google Scholar
Heuman, DM (1989) Quantitative estimation of the hydrophilic–hydrophobic balance of mixed bile salt solutions. Journal of Lipid Research 30, 719730.CrossRefGoogle ScholarPubMed
Huet, S, Bouvier, A, Gruet, MA & Jolivet, E (1996) Statistical Tools for Nonlinear Regression. A Practical Guide with S-PLUS Examples. New York, NY: Springer Verlag.CrossRefGoogle Scholar
Juste, C, Catala, I, Auboiron, S, Fiszelewicz, M, Fénart, E, Peyronnet, C & Corring, T (1997 a) Effects of dietary proteins on serum and biliary lipids and on cholesterol precipitation from pig bile. In Proceedings of the VIIth International Symposium on Digestive Physiology in Pigs, pp. 2832. [Laplace, JP, Février, C and Barbeau, A, editors]. Rome: EAAP.Google Scholar
Juste, C, Catala, I, Henry, R, Chabanet, C, Gueugneau, AMBéguet, F, Lyan, B and Corring, T (1995) Influence of bile salt molecular species on cholesterol crystallization from supersaturated model biles. Biochimica et Biophysica Acta 1254, 8997.CrossRefGoogle ScholarPubMed
Juste, C, Catala, I, Riottot, MAndré, M, Parquet, M, Lyan, BBéguet, F, Férézou, J, Sérougne, C, Domingo, N, Lutton, C, Lafont, H and Corring, T (1997) Inducing cholesterol precipitation from pig bile with β-cyclodextrin and cholesterol dietary supplementation. Journal of Hepatology 26, 711721.CrossRefGoogle ScholarPubMed
Kern, F (1994) Effects of dietary cholesterol on cholesterol and bile acid homeostasis in patients with cholesterol gallstones. Journal of Clinical Investigation 93, 11861194.CrossRefGoogle ScholarPubMed
Kim, DN, Lee, KT, Reiner, JM and Thomas, WA (1978) Effects of a soy protein product on serum and tissue cholesterol concentrations in swine fed high-fat, high-cholesterol diets. Experimental Molecular Pathology 29, 385399.CrossRefGoogle ScholarPubMed
Kim, DN, Lee, KT, Reiner, JM and Thomas, WA (1980) Increased steroid excretion in swine fed high-fat, high-cholesterol diet with soy protein. Experimental Molecular Pathology 33, 2535.CrossRefGoogle ScholarPubMed
Konikoff, FM, Cohen, DE and Carey, MC (1994) Phospholipid molecular species influence crystal habits and transition sequences of metastable intermediates during cholesterol crystallization from bile salt-rich model bile. Journal of Lipid Research 35, 6070.CrossRefGoogle ScholarPubMed
Kritchevsky, D and Klurfeld, DM (1983) Gallstone formation in hamsters: effect of varying animal and vegetable protein levels. American Journal of Clinical Nutrition 37, 802804.CrossRefGoogle ScholarPubMed
Legrand-Defretin, V, Juste, C, Henry, R and Corring, T (1991) Ion-pair high performance liquid chromatography of bile salt conjugates: application to pig bile. Lipids 26, 578583.CrossRefGoogle ScholarPubMed
Leonardi, J, Termine, E, Morand, F, Lafont, R, Portugal, H, Lafont, H and Nalbone, G (1987) Effect of dietary lipids on the lipid composition and phospholipid deacylating enzyme activities of rat heart. Lipids 22, 517522.CrossRefGoogle ScholarPubMed
Marsh, A, Kim, DN, Lee, KT, Reiner, JM and Thomas, WA (1972) Cholesterol turnover, synthesis, and retention in hypocholesterolemic growing swine. Journal of Lipid Research 13, 600615.CrossRefGoogle Scholar
Newburgh, LH and Clarkson, S (1923) The production of atherosclerosis in rabbits by feeding diets rich in meat. Archives of Internal Medicine 31, 653676.CrossRefGoogle Scholar
Ozben, T (1989) Biliary lipid composition and gallstone formation in rabbits fed on soy protein, cholesterol, casein and modified casein. Biochemical Journal 263, 293296.CrossRefGoogle ScholarPubMed
Pixley, F, Wilson, DMcPherson, K and Mann, J (1985) The effect of vegetarianism on development of gallstones in women. British Medical Journal 91, 1112.CrossRefGoogle Scholar
Potter, SM (1995) Overview of proposed mechanisms for the hypocholesterolemic effect of soy. Journal of Nutrition 125, 606S611S.Google ScholarPubMed
Prosky, L, Asp, NG, Schweizer, TF, De Vries, JW and Furda, I (1988) Determination of insoluble, soluble, and total dietary fiber in foods and food products: interlaboratory study. Journal of the Association of Official Analytical Chemists 71, 10171023.Google ScholarPubMed
Riottot, M, Olivier, P, Huet, ACaboche, J-J, Parquet, M, Khallou, J and Lutton, C (1993) Hypolipidemic effects of β-cyclodextrin in the hamster and in the genetically hypercholesterolemic Rico rat. Lipids 28, 181188.CrossRefGoogle ScholarPubMed
Salvioli, G, Igimi, M and Carey, M (1983) Cholesterol gallstone dissolution in bile. Dissolution kinetics of crystalline cholesterol monohydrate by conjugated chenodeoxycholate–lecithin mixtures: dissimilar phase equilibria and dissolution mechanism. Journal of Lipid Research 24, 701720.CrossRefGoogle Scholar
Scholz, K-E, Kinder, E, Hagemeister, H and Barth, CA (1985) Influence of dietary casein and soy protein isolate on intestinal cholesterol and bile acid concentration. Zeitschrift fur Ernahrungswissenschaft 24, 158171.CrossRefGoogle ScholarPubMed
Scobey, MW, Johnson, FL, Parks, JS and Rudel, LL (1991) Dietary fish oil effects on biliary lipid secretion and cholesterol gallstone formation in the African green monkey. Hepatology 14, 679684.Google ScholarPubMed
Singleton, WS, Gray, MS, Brown, MI and White, JL (1965) Chromatographically homogeneous lecithin from egg phospholipids. Journal of the American Oil Chemists' Society 42, 5356.CrossRefGoogle ScholarPubMed
Stolk, MFJ, Van de Heijning, BJM, van Erpecum, KJvan den Broek, AMWC, Renooij, W and van Berge-Henegouwen, GP (1994) The effect of bile acid hydrophobicity on nucleation of several types of cholesterol crystals from model bile vesicles. Journal of Hepatology 20, 802810.CrossRefGoogle ScholarPubMed
Sullivan-Gorman, MA, Duffy, ADiMarco, NM and Liepa, G (1985) Effects of various dietary animal and vegetable proteins on serum and biliary lipids and on gallstone formation in the hamster. Lipids 20, 16.CrossRefGoogle Scholar
Tanaka, K, Aso, B and Sugano, M (1984) Biliary steroid excretion in rats fed soybean protein and casein or their amino acid mixtures. Journal of Nutrition 114, 2632.CrossRefGoogle ScholarPubMed
Tazuma, S, Ochi, H, Teramen, K, Yamashita, Y, Horikawa, K, Miura, H, Hirano, N, Sasaki, M, Aihara, N, Hatsushika, S, Tao, S, Ohya, T and Kajiyama, G (1994) Degree of fatty acyl chain unsaturation in biliary lecithin dictates cholesterol nucleation and crystal growth. Biochimica et Biophysica Acta 1215, 7478.CrossRefGoogle ScholarPubMed
Terpstra, AHM, Harkes, L and van der Veen, FH (1981) The effect of different proportions of casein in semipurified diets on the concentration of serum cholesterol and the lipoprotein composition in rabbits. Lipids 16, 114119.CrossRefGoogle ScholarPubMed
Terpstra, AHM, Laitinen, L, Stucchi, AF and Nicolosi, RJ (1994) The effect of semipurified diets containing two levels (20 % and 40 %) of either casein or soybean protein isolate and concentrate on plasma lipids in hamsters. Nutrition Research 14, 885895.CrossRefGoogle Scholar
Trautwein, EA, Liang, J and Hayes, KC (1993) Cholesterol gallstone induction in hamsters reflects strain differences in plasma lipoproteins and bile acid profiles. Lipids 28, 305312.CrossRefGoogle ScholarPubMed
van de Heijning, BJM, Stolk, MFJ, van Erpecum, KJ, Renooij, W and van Berge-Henegouwen, GP (1995) The effects of bile salt hydrophobicity on model bile vesicle morphology. Biochimica et Biophysica Acta 1212, 203210.CrossRefGoogle Scholar
van der Meer, R and Beynen, AC (1987) Species-dependent responsiveness of serum cholesterol to dietary proteins. Journal of the American Oil Chemists' Society 64, 11721177.CrossRefGoogle Scholar